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The following tactics are described for control of aphids as virus vectors; chemical control (repellents, feeding deterrents, alarm pheromone, insecticides), physical control (mulch, fleece, netting) and biological control (insect parasitoids and predators). No tactic is able to protect plants completely against virus infections when used alone, except for certain fleeces. Multiple tactics must be used to build integrated pest management programs (IPM).
Abstracts in Other Languages: 中文, 日本語, 한국어
This paper reviews recent work on tactics for controlling vector aphids to protect plants against virus infection. I hope it will contribute to the development of an effective strategy against the viruses, which cause serious damage to tropical crops. Such viruses include banana bunchy top virus (BBTV) and papaya ringspot virus (PRSV).
This compound, isolated from water-pepper (Polygonum hydropiper), is a sesquiterpenoid which is highly repellent to aphids (Asakawa et al. 1988, Griffiths et al. 1989). Extraction of (-)-polygodial from the plant yielded material for a field trial to test the level of protection against barley yellow dwarf virus (BYDV), transmitted by the aphid Rhopalosiphum padi. Under conditions of high pest and disease pressure, three two-weekly treatments of this compound at 50 g/ha increased the yield by over 1 mt/ha. This is similar to the control achieved by the conventional broad-spectrum insecticide cypermethrin (Pickett et al. 1992).
This triterpenoid, isolated from the neem tree (Azadirachta indica), reduced probing activity by R. padi and Sitobion avenae on winter barley treated with concentrations of <500 ppm. The effect lasted for at least four days after application (West and Mordue 1992). The reduction in probing activity would diminish the probability of BYDV transmission by these aphids.
Applying the alarm pheromone (E)-beta-farnesene has not been effective, because it makes the aphids more active, and might increase transmission of viruses. However, a spray application of carbamate or organic phosphate, at one-tenth of the recommended dose, in combination with the pheromone, was successful in controlling aphids on iceberg lettuce (Ester et al. 1993). It thus seems to be possible to diminish virus transmission by aphids by using an insecticide in combination with the pheromone.
Compounds derived from the alarm pheromone can affect aphid settling and feeding, and decrease virus spread both in the laboratory and in the field (Dawson et al. 1988, Griffiths et al. 1989).
An alternative way of using alarm pheromone is to disrupt effective alarm communication between aphids, by the presence of a high background level of synthetic alarm pheromone. Under these conditions, predators may become more effective in feeding on aphids. However, this hypothesis was not supported by the experimental results of E1-Agamy and Haynes (1992) when they worked with the predator Navis americoferus. The potential role of habituation or sensory adaptation is well worth further investigation.
Certain mineral oils are known to reduce aphid colonization on plants, and thus the transmission of virus disease (Simons and Zitter 1980). Vandenveken (1977) suggested two hypotheses for the effect of oils on aphid transmission of plant viruses. One is that oil might modify the charge of the stylets, thus impeding adsorption or elusion of virus particles. The second is that the inhibitory properties of oils might result from their electric insulating properties, which would hamper the exchange of charges between virus particles, aphid mouthparts and plant cells.
The pyrethroid deltamethrin inhibits virus transmission by the green peach aphid Myzus persicae by causing rapid knock-down and prolonged incapacitation of the insect (Gibson et al. 1982). In laboratory tests with moderately pyrethroid-resistant (R1) M. persicae, more of the aphids walked or flew from excised leaves pre-treated with deltamethrin than from untreated leaves. R1 alatae and apterae which had dispersed from deltamethrin-treated leaves rarely transmitted potato virus Y (PVY). However, transmission by the more pyrethroid-resistant R2 alatae was only halved, although transmission by R2 apterae was undiminished. Treatment with deltamethrin decreased the spread of PVY both in a flight chamber, and in field experiments (Rice et al. 1983).
Conventional insecticide treatments are not necessarily effective in preventing the introduction and subsequent field spread of non-persistent viruses. However, if naturally beneficial insects cannot suppress the population density of the vector aphid, the use of insecticides cannot be avoided. In such cases, insecticides with highly selective activity on the aphid and its natural enemies, such as certain systemic aphicides or sodium oleate, should be used.
Kring (1964) first reported that short-wave-length radiation repelled aphids after a dispersal flight. Reflective (silver) mulch reduced aphid populations and virus incidence, and increased the yields of crops (Pinese et al. 1994). A new plastic mulch with a reflective mirror-like surface, called "mirror mulch", has recently been developed in Japan. When mirror mulch was laid between rows in tobacco fields, populations of alate aphids in water traps were significantly lower, and a lower proportion of plants were diseased by potato virus Y-T strain (PVY-T), compared to treatments of silver mulch under the plants (Matsuzawa 1995).
Various types of plant covers have been suggested as a promising way of reducing virus transmission by aphids. Even though the aphid cannot pass through these covers, the question still remains of whether penetration of leaves by the aphid's stylets may occur if the leaves are in close contact with the cover. One successful penetration per plant is sufficient for virus transmission by an aphid. Field experiments with potato showed that one particular fleece (Lutrasil) completely protected the plants against virus transmission (PVY and PLRV). The use of a second type of fleece (Agrifleece) and netting (Rantai, 19 mesh) resulted in a small proportion of plants being infected (Harrewijn et al. 1991). A field of tobacco covered with a fleece (possibly Lutrasil) for 50 days after transplantation was fully protected against virus transmission (Tairako 1989).
It is difficult to utilize insect natural enemies of aphids for virus disease control. This is particularly true when the pathogenic virus is transmitted in a non-persistent manner by several species, as is the case with papaya ringspot virus (PRSV). Vector aphids of PRSV include the polyphagous species Myzus persicae and Aphis gossypii, both of which occur on many species of plants, not only in the open field but also in scrub, orchards and gardens. On the other hand, insect natural enemies can contribute to the control of a virus disease in cases where the pathogenic virus is transmitted in a semi-persistent or persistent manner by a particular aphid species. Banana bunchy-top virus (BBTV) is such a case. This virus is transmitted in a semi-persistent manner only by the banana aphid, Pentalonia nigronervosa.
Three programs of biological control of P. nigronervosa have been attempted. In Western Samoa, two species of coccinellid predators were used in a single program (Waterhause and Norris 1987), while in Tonga, two aphidiid parasitoids were used in succession. The first was Lysiphlebus testaceipes in 1987 (Stechmann and Voelkl 1988), and the second was Aphidius colemani in 1990-91 (Wellings et al. 1994). The first two programs have produced no evidence that any of the introduced agents have become established. The third program has not provided any evidence that the parasitoid is attacking P. nigronervosa in the field. However, A. colemani was recovered from Aphis gossypii on taro about nine months after the last release. In August 1992, the dissection of A. gossypii collected from two taro sites revealed parasitism rates of 47% and 39%, respectively. P. nigronervosa collected from banana growing on the margins of the two taro fields showed no parasitization when they were dissected (Wellings et al. 1994). Wellings et al. (1994) supposed that the heavy attendance of ants on P. nigronervosa colonies might well be preventing attack by the parasitoid. Alternatively, the parasitoid may be demonstrating an inherent preference for aphid species other than P. nigronervosa in the field.
Only two aphidiid species have been recorded so far to be natural parasitoids of P. nigronervosa. These are Lipolexis scutellaris from Taiwan (Chou 1984) and Lysiphlebus testaceipes from Cuba (Stary 1966). Four aphidiid species (Ephedrus plagiator, Aphidius colemani, Lysiphlebus fabarum (Voelkl et al. 1990), and Ephedrus cerasicola (Stary and Stechmann 1990)) were confirmed as potentially suitable parasitoids of P. nigronervosa. Furthermore, an aphidiid and two aphelinid species (Lysiphlebus japonicus, Aphelinus gossypii and Aphelinus sp. nr. varipes) were successfully propagated on P. nigronervosa on banana suckers in a laboratory (Takada, unpublished data). Of these species, L. testaceipes and A. colemani have been used in a practical biological control program, as mentioned above. L. scutellaris and other potential parasitoids may be useful.
A total of about ten species belonging to Coccinellidae, Syrphidae, Chrysopidae and Hemerobiidae have been recorded as predators of P. nigronervosa (Tao 1990; Carver et al. 1993). Among these predators I think hemerobiids are the most promising agents for the biological control of the aphid. This is because larvae of hemerobiids tend to search and stay on concealed parts of the plant. Small colonies of this aphid thus feed mainly on concealed parts such as the areas between the leaf sheaths and the pseudostem of the banana plant.
From the viewpoint of virus disease control, there are two strategies for vector aphid control.
Direct Strategies: to prevent virus acquisition and transmission by vector aphids
Indirect Strategies: to reduce the population density of vector aphids (insecticides, insect natural enemies)
None of the tactics mentioned above is able to protect plants completely against virus infection when used alone, except for certain fleeces. Multiple tactics must be used, to build integrated pest management programs (IPM). Pinese et al. (1994) evaluated two insecticides, two mineral oil sprays and different-colored reflective mulches, alone and in combination, for the control of PRSV in zucchini (Cucurbita pepo) in Australia. A treatment strategy incorporating the repellent qualities of reflective silver mulches against itinerant aphid vectors, plus the protectant qualities of non-phytotoxic mineral oils and deltamethrin sprays to reduce the number of vectors on crops, provided the best control options. It may be possible to apply a similar strategy successfully to other crops susceptible to viruses.
Dr. Takada was asked how the mineral oil was used, and explained that it was sprayed on the leaves. Dr. Kiritani, former deputy Director of the Center, commented that at this meeting on insect-borne virus diseases, most participants were plant pathologists and virologists. However, control must be based on an understanding of the insect vectors, and he had appreciated very much the input of an entomologist such as Dr. Takada.
Transmission of aphid-borne virus diseases depends on the winged or alate form of aphid, and Dr. Kiritani asked whether it is possible to reduce the numbers of the winged type so that there is a lower incidence of virus diseases. Dr. Takada pointed out that the winged type of aphid is seasonal: in a temperate climate with pronounced seasonality, the number of winged forms is high in spring and autumn. In summer, the incidence of winged forms depends on the population density of the aphid. If the population density is reduced by chemical sprays or natural enemies, the incidence of winged forms should also be reduced.
Several participants were interested in the mirror mulch, and asked whether many growers in Japan are using it, how it is applied, and whether it is very expensive. Dr. Takada replied that not many growers have adopted the use of mirror mulch so far, at most 12% in the area, but that its use is on the increase. Mirror mulch is more expensive than silver mulch, but it is cost effective. It not only controls aphids and the diseases they vector, but produces good leaf tobacco by reflecting the light up into the lower leaves. It is applied to alternate rows in the tobacco field, not beneath the plant in the way that silver mulch is used.
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